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Genomics of clownfish adaptation to sea anemones: investigating the genetic bases of the acquisition of the mutualism and the diversification along host usage and habitat gradients

Anna Marcionetti1*, Victor Rossier1, Natach Roux2, Pauline Salis1, Vincent Laudet2 and Nicolas Salamin1
  • 1 Département de biologie computationnelle, Faculté de biologie et de médecine, université de Lausanne, Switzerland
  • 2 Observatoire Océanologique de Banyuls, France

Clownfishes (family Pomacentridae, genera Amphiprion and premnas) are an iconic group of coral reef fishes distributed in the tropical belt of the Indo-Pacific Ocean, and it includes 26 currently recognized species and 2 natural hybrids (Fautin & Allen, 1997; Ollerton et al. 2007; Gainsford et al. 2015). A distinctive characteristic of this group is the mutualistic interaction they maintain with sea anemones (Fautin & Allen, 1997). This mutualism acted as the key innovation that triggered clownfish adaptive radiation. Indeed, after the acquisition of the mutualism, clownfishes experienced rapid and convergent morphological changes that are correlated with the different ecological niches offered by the host anemones (i.e. host usage as the number of possible sea anemone hosts and habitat as substrate and depth; Litsios et al. 2012). This diversification along host usage and habitat gradients happened independently in many closely related clownfish species, providing replicated systems that have followed similar routes during the adaptive radiation. Despite the importance of this mutualism in the diversification of clownfishes, the genetic and genomic mechanisms that allowed them to interact with sea anemones are still unclear. Sea anemones are sessile organisms that have evolved a variety of toxins used for protection and hunting, which can be extremely harmful to the fishes (Nedosyko et al., 2014). These toxins are released from specialized cells (i.e. cnidocytes) after the combination of chemical and mechanical stimuli (Anderson & Bouchard, 2009), or they are secreted in the mucus of sea anemones (Mebs, 2009). Thus, clownfishes must have evolved specific characteristics to counteract these toxins. We can today take advantage of next-generation sequencing technologies to obtain genomes of different clownfish species to better understand the mechanisms of clownfish adaptation to sea anemones. By considering the mutualism as a new and advantageous phenotype that evolved in clownfishes, we can investigate the role of selection on the genetic basis of the adaptation. Indeed, phenotypic evolution may occur through alterations of the structure of protein-coding genes, which can be fixed by positive selection if they confer an advantage (as for example in Spady et al., 2005; Hoekstra et al., 2006; Protas et al. 2006; Lynch, 2007). In this project, we obtained genomic data for ten clownfish species and tested the genetic mechanisms underlying clownfish protection from sea anemone toxins using comparative genomics and molecular evolution analyses (Marcionetti et al., 2019). The 10 selected clownfish species form five pairs of closely-related but ecologically-divergent species in their host and habitat usage. This design does not only allow to investigate patterns of positive selection at the origin of the clownfish group, but it also allows to study whether the same genes were positively selected during the independent adaptation of different clownfish species to similar sea anemones hosts. After the genome assembly and annotation of the clownfish genomes, we inferred orthologous genes between these species and other publicly-available teleost genomes. This resulted in a total of 15,940 orthologous groups that were tested for the presence of positively-selected substitutions on protein-coding genes that may be linked with clownfish adaptation to sea anemones. We identified 19 genes with a signal of positive selection at the origin of clownfishes. Two of them (Versican core protein and Protein O-GlcNAse) show particularly interesting functions associated with N-acetylated sugars, which are known to be involved in sea anemone discharge of toxins (Marcionetti et al., 2019). We also found patterns of positive selection associated with the divergence of host usage. Thus, these genes may be linked to the adaptation of specific clownfish species to different sea anemones hosts. This project provides the first insights into the genetic mechanisms of clownfish mutualism with sea anemones. Although a causal link cannot be confirmed without further experimental validation, we identified the first candidate genes that are likely to be associated with clownfish protection form sea anemones, and thus the evolution of their mutualism.

References

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Keywords: Anemonefish, Amphiprion, Coral reef fish, positive selection, key-innovation

Conference: XVI European Congress of Ichthyology, Lausanne, Switzerland, 2 Sep - 6 Sep, 2019.

Presentation Type: Oral

Topic: EVOLUTIONARY GENOMICS OF FISHES

Citation: Marcionetti A, Rossier V, Roux N, Salis P, Laudet V and Salamin N (2019). Genomics of clownfish adaptation to sea anemones: investigating the genetic bases of the acquisition of the mutualism and the diversification along host usage and habitat gradients. Front. Mar. Sci. Conference Abstract: XVI European Congress of Ichthyology. doi: 10.3389/conf.fmars.2019.07.00042

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Received: 20 Jul 2019; Published Online: 14 Aug 2019.

* Correspondence: Ms. Anna Marcionetti, Département de biologie computationnelle, Faculté de biologie et de médecine, université de Lausanne, Lausanne, Vaud, 1011, Switzerland, anna.marcionetti@unil.ch